The Kinetics of Electron Transfer from CdS Nanorods to the MoFe Protein of Nitrogenase
Abstract
Combining the remarkable catalytic properties of redox enzymes with highly tunable light absorbing properties of semiconductor nanocrystals enables the light-driven catalysis of complex, multielectron redox reactions. This work focuses on systems that combine CdS nanorods (NRs) with the MoFe protein of nitrogenase to drive photochemical N2 reduction. We used transient absorption spectroscopy (TAS) to examine the kinetics of electron transfer (ET) from CdS NRs to the MoFe protein. For CdS NRs with dimensions similar to those previously used for photochemical N2 reduction, the rate constant for ET from CdS NRs competes with other electron relaxation processes, such that when a MoFe protein is bound to a NR, about one-half of the photoexcited electrons are delivered to the enzyme. The NR-MoFe protein binding is incomplete with more than one-half of the NRs in solution not having a MoFe protein bound to accept electrons. The quantum efficiency of ET (QEET) in these ensemble samples is similar to previously reported efficiencies of product (NH3 and H2) formation, suggesting that the enzyme utilizes the delivered electrons without major loss pathways. Our analysis suggests that QEET, and therefore the photochemical product formation, is limited at the ensemble level by the NR-MoFe protein binding and atmore »
- Authors:
-
- Univ. of Colorado, Boulder, CO (United States)
- Utah State Univ., Logan, UT (United States)
- Washington State Univ., Pullman, WA (United States); Montana State Univ., Bozeman, MT (United States)
- National Renewable Energy Lab. (NREL), Golden, CO (United States)
- Washington State Univ., Pullman, WA (United States)
- National Renewable Energy Lab. (NREL), Golden, CO (United States); Univ. of Colorado, Boulder, CO (United States)
- Publication Date:
- Research Org.:
- National Renewable Energy Lab. (NREL), Golden, CO (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division; National Science Foundation (NSF)
- OSTI Identifier:
- 1872406
- Report Number(s):
- NREL/JA-2700-81982
Journal ID: ISSN 1932-7447; MainId:82755;UUID:5e9c4e30-8394-4359-8e7a-fa288a6e0594;MainAdminID:64669
- Grant/Contract Number:
- AC36-08GO28308; CHE-2125978
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Journal of Physical Chemistry. C
- Additional Journal Information:
- Journal Volume: 126; Journal Issue: 19; Journal ID: ISSN 1932-7447
- Publisher:
- American Chemical Society
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; ammonia production; biohybrid; electron transfer; nanocrystal; solar fuels
Citation Formats
Ruzicka, Jesse L., Pellows, Lauren M., Kallas, Hayden, Shulenberger, Katherine E., Zadvornyy, Oleg A., Chica, Bryant, Brown, Katherine A., Peters, John W., King, Paul W., Seefeldt, Lance C., and Dukovic, Gordana. The Kinetics of Electron Transfer from CdS Nanorods to the MoFe Protein of Nitrogenase. United States: N. p., 2022.
Web. doi:10.1021/acs.jpcc.2c02528.
Ruzicka, Jesse L., Pellows, Lauren M., Kallas, Hayden, Shulenberger, Katherine E., Zadvornyy, Oleg A., Chica, Bryant, Brown, Katherine A., Peters, John W., King, Paul W., Seefeldt, Lance C., & Dukovic, Gordana. The Kinetics of Electron Transfer from CdS Nanorods to the MoFe Protein of Nitrogenase. United States. https://doi.org/10.1021/acs.jpcc.2c02528
Ruzicka, Jesse L., Pellows, Lauren M., Kallas, Hayden, Shulenberger, Katherine E., Zadvornyy, Oleg A., Chica, Bryant, Brown, Katherine A., Peters, John W., King, Paul W., Seefeldt, Lance C., and Dukovic, Gordana. Mon .
"The Kinetics of Electron Transfer from CdS Nanorods to the MoFe Protein of Nitrogenase". United States. https://doi.org/10.1021/acs.jpcc.2c02528. https://www.osti.gov/servlets/purl/1872406.
@article{osti_1872406,
title = {The Kinetics of Electron Transfer from CdS Nanorods to the MoFe Protein of Nitrogenase},
author = {Ruzicka, Jesse L. and Pellows, Lauren M. and Kallas, Hayden and Shulenberger, Katherine E. and Zadvornyy, Oleg A. and Chica, Bryant and Brown, Katherine A. and Peters, John W. and King, Paul W. and Seefeldt, Lance C. and Dukovic, Gordana},
abstractNote = {Combining the remarkable catalytic properties of redox enzymes with highly tunable light absorbing properties of semiconductor nanocrystals enables the light-driven catalysis of complex, multielectron redox reactions. This work focuses on systems that combine CdS nanorods (NRs) with the MoFe protein of nitrogenase to drive photochemical N2 reduction. We used transient absorption spectroscopy (TAS) to examine the kinetics of electron transfer (ET) from CdS NRs to the MoFe protein. For CdS NRs with dimensions similar to those previously used for photochemical N2 reduction, the rate constant for ET from CdS NRs competes with other electron relaxation processes, such that when a MoFe protein is bound to a NR, about one-half of the photoexcited electrons are delivered to the enzyme. The NR-MoFe protein binding is incomplete with more than one-half of the NRs in solution not having a MoFe protein bound to accept electrons. The quantum efficiency of ET (QEET) in these ensemble samples is similar to previously reported efficiencies of product (NH3 and H2) formation, suggesting that the enzyme utilizes the delivered electrons without major loss pathways. Our analysis suggests that QEET, and therefore the photochemical product formation, is limited at the ensemble level by the NR-MoFe protein binding and at the single-complex level by the competitiveness of ET. We characterized ET kinetics for several CdS NRs samples with varying dimensions and found that for CdS NRs with an average diameter of 4.2 nm the ET efficiency dropped to undetectable levels, defining a maximum NR diameter that should be used to photochemically drive the MoFe protein. The work described here provides insights into the design of systems with increased control of photochemical N2 reduction catalyzed by the MoFe protein of nitrogenase.},
doi = {10.1021/acs.jpcc.2c02528},
journal = {Journal of Physical Chemistry. C},
number = 19,
volume = 126,
place = {United States},
year = {2022},
month = {5}
}
Works referenced in this record:
Ligand Effects on Optical Properties of CdSe Nanocrystals
journal, April 2005
- Kalyuzhny, Gregory; Murray, Royce W.
- The Journal of Physical Chemistry B, Vol. 109, Issue 15
Quantum Efficiency of Charge Transfer Competing against Nonexponential Processes: The Case of Electron Transfer from CdS Nanorods to Hydrogenase
journal, December 2018
- Utterback, James K.; Wilker, Molly B.; Mulder, David W.
- The Journal of Physical Chemistry C, Vol. 123, Issue 1
DLS and zeta potential – What they are and what they are not?
journal, August 2016
- Bhattacharjee, Sourav
- Journal of Controlled Release, Vol. 235
Diameter Dependent Electron Transfer Kinetics in Semiconductor–Enzyme Complexes
journal, October 2014
- Brown, Katherine A.; Song, Qing; Mulder, David W.
- ACS Nano, Vol. 8, Issue 10
Defining Intermediates of Nitrogenase MoFe Protein during N 2 Reduction under Photochemical Electron Delivery from CdS Quantum Dots
journal, July 2020
- Chica, Bryant; Ruzicka, Jesse; Kallas, Hayden
- Journal of the American Chemical Society, Vol. 142, Issue 33
Catalytic and Biophysical Properties of a Nitrogenase Apo-MoFe Protein Produced by a n ifB -Deletion Mutant of Azotobacter v inelandii †
journal, September 1998
- Christiansen, Jason; Goodwin, Paul J.; Lanzilotta, William N.
- Biochemistry, Vol. 37, Issue 36
Experimental Determination of the Extinction Coefficient of CdTe, CdSe, and CdS Nanocrystals
journal, July 2003
- Yu, W. William; Qu, Lianhua; Guo, Wenzhuo
- Chemistry of Materials, Vol. 15, Issue 14, p. 2854-2860
Nitrogenase Bioelectrocatalysis: ATP-Independent Ammonia Production Using a Redox Polymer/MoFe Protein System
journal, June 2020
- Lee, Yoo Seok; Yuan, Mengwei; Cai, Rong
- ACS Catalysis, Vol. 10, Issue 12
Nitrogenase MoFe-Protein at 1.16 A Resolution: A Central Ligand in the FeMo-Cofactor
journal, September 2002
- Einsle, O.
- Science, Vol. 297, Issue 5587
Spectroscopic Evidence for the Contribution of Holes to the Bleach of Cd-Chalcogenide Quantum Dots
journal, March 2019
- Grimaldi, Gianluca; Geuchies, Jaco J.; van der Stam, Ward
- Nano Letters, Vol. 19, Issue 5
Infrared spectroscopy of the nitrogenase MoFe protein under electrochemical control: potential-triggered CO binding
journal, January 2017
- Paengnakorn, P.; Ash, P. A.; Shaw, S.
- Chemical Science, Vol. 8, Issue 2
Nature of biological electron transfer
journal, February 1992
- Moser, Christopher C.; Keske, Jonathan M.; Warncke, Kurt
- Nature, Vol. 355, Issue 6363
Light-driven carbon−carbon bond formation via CO 2 reduction catalyzed by complexes of CdS nanorods and a 2-oxoacid oxidoreductase
journal, December 2019
- Hamby, Hayden; Li, Bin; Shinopoulos, Katherine E.
- Proceedings of the National Academy of Sciences, Vol. 117, Issue 1
Observation of trapped-hole diffusion on the surfaces of CdS nanorods
journal, July 2016
- Utterback, James K.; Grennell, Amanda N.; Wilker, Molly B.
- Nature Chemistry, Vol. 8, Issue 11
Mechanism of Nitrogen Fixation by Nitrogenase: The Next Stage
journal, January 2014
- Hoffman, Brian M.; Lukoyanov, Dmitriy; Yang, Zhi-Yong
- Chemical Reviews, Vol. 114, Issue 8
Crystallographic structure of the nitrogenase iron protein from Azotobacter vinelandii
journal, September 1992
- Georgiadis, M.; Komiya, H.; Chakrabarti, P.
- Science, Vol. 257, Issue 5077
Natural engineering principles of electron tunnelling in biological oxidation–reduction
journal, November 1999
- Page, Christopher C.; Moser, Christopher C.; Chen, Xiaoxi
- Nature, Vol. 402, Issue 6757
Balancing electron transfer rate and driving force for efficient photocatalytic hydrogen production in CdSe/CdS nanorod–[NiFe] hydrogenase assemblies
journal, January 2017
- Chica, Bryant; Wu, Chang-Hao; Liu, Yuhgene
- Energy & Environmental Science, Vol. 10, Issue 10
Electron Transfer from Semiconductor Nanocrystals to Redox Enzymes
journal, April 2020
- Utterback, James K.; Ruzicka, Jesse L.; Keller, Helena R.
- Annual Review of Physical Chemistry, Vol. 71, Issue 1
Tailoring electron transfer pathway for photocatalytic N 2 -to-NH 3 reduction in a CdS quantum dots-nitrogenase system
journal, January 2022
- Badalyan, Artavazd; Yang, Zhi-Yong; Hu, Maowei
- Sustainable Energy & Fuels, Vol. 6, Issue 9
Temperature-Dependent Transient Absorption Spectroscopy Elucidates Trapped-Hole Dynamics in CdS and CdSe Nanorods
journal, May 2019
- Utterback, James K.; Ruzicka, Jesse L.; Hamby, Hayden
- The Journal of Physical Chemistry Letters, Vol. 10, Issue 11
Investigating Protein–Nanocrystal Interactions for Photodriven Activity
journal, January 2020
- Harris, Alexander W.; Harguindey, Albert; Patalano, Ryan E.
- ACS Applied Bio Materials, Vol. 3, Issue 2
Characterization of Photochemical Processes for H 2 Production by CdS Nanorod–[FeFe] Hydrogenase Complexes
journal, March 2012
- Brown, Katherine A.; Wilker, Molly B.; Boehm, Marko
- Journal of the American Chemical Society, Vol. 134, Issue 12
On the Origin of Surface Traps in Colloidal II–VI Semiconductor Nanocrystals
journal, January 2017
- Houtepen, Arjan J.; Hens, Zeger; Owen, Jonathan S.
- Chemistry of Materials, Vol. 29, Issue 2
Excitation-Rate Determines Product Stoichiometry in Photochemical Ammonia Production by CdS Quantum Dot-Nitrogenase MoFe Protein Complexes
journal, September 2020
- Brown, Katherine A.; Ruzicka, Jesse; Kallas, Hayden
- ACS Catalysis, Vol. 10, Issue 19
Competition between electron transfer, trapping, and recombination in CdS nanorod–hydrogenase complexes
journal, January 2015
- Utterback, James K.; Wilker, Molly B.; Brown, Katherine A.
- Physical Chemistry Chemical Physics, Vol. 17, Issue 8
Large-scale purification of high activity Azotobacter vinelandii nitrogenase
journal, July 1980
- Burgess, Barbara K.; Jacobs, Deloria B.; Stiefel, Edward I.
- Biochimica et Biophysica Acta (BBA) - Enzymology, Vol. 614, Issue 1
Merck molecular force field. I. Basis, form, scope, parameterization, and performance of MMFF94
journal, April 1996
- Halgren, Thomas A.
- Journal of Computational Chemistry, Vol. 17, Issue 5-6
Electron–electron and electron‐hole interactions in small semiconductor crystallites: The size dependence of the lowest excited electronic state
journal, May 1984
- Brus, L. E.
- The Journal of Chemical Physics, Vol. 80, Issue 9
Electron Transfer within Nitrogenase: Evidence for a Deficit-Spending Mechanism
journal, November 2011
- Danyal, Karamatullah; Dean, Dennis R.; Hoffman, Brian M.
- Biochemistry, Vol. 50, Issue 43
NIH Image to ImageJ: 25 years of image analysis
journal, June 2012
- Schneider, Caroline A.; Rasband, Wayne S.; Eliceiri, Kevin W.
- Nature Methods, Vol. 9, Issue 7
ATP- and Iron−Protein-Independent Activation of Nitrogenase Catalysis by Light
journal, October 2010
- Roth, Lauren E.; Nguyen, Joey C.; Tezcan, F. Akif
- Journal of the American Chemical Society, Vol. 132, Issue 39
ATP-Uncoupled, Six-Electron Photoreduction of Hydrogen Cyanide to Methane by the Molybdenum–Iron Protein
journal, May 2012
- Roth, Lauren E.; Tezcan, F. Akif
- Journal of the American Chemical Society, Vol. 134, Issue 20
Electronic landscape of the P-cluster of nitrogenase as revealed through many-electron quantum wavefunction simulations
journal, September 2019
- Li, Zhendong; Guo, Sheng; Sun, Qiming
- Nature Chemistry, Vol. 11, Issue 11
Linking surface chemistry to optical properties of semiconductor nanocrystals
journal, January 2015
- Krause, Michael M.; Kambhampati, Patanjali
- Physical Chemistry Chemical Physics, Vol. 17, Issue 29
Long-range electron transfer
journal, February 2005
- Gray, H. B.; Winkler, J. R.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 10
Nitrogenase bioelectrocatalysis: heterogeneous ammonia and hydrogen production by MoFe protein
journal, January 2016
- Milton, Ross D.; Abdellaoui, Sofiene; Khadka, Nimesh
- Energy & Environmental Science, Vol. 9, Issue 8
Ligand Exchange and the Stoichiometry of Metal Chalcogenide Nanocrystals: Spectroscopic Observation of Facile Metal-Carboxylate Displacement and Binding
journal, November 2013
- Anderson, Nicholas C.; Hendricks, Mark P.; Choi, Joshua J.
- Journal of the American Chemical Society, Vol. 135, Issue 49, p. 18536-18548
Cluster-Dependent Charge-Transfer Dynamics in Iron–Sulfur Proteins
journal, January 2018
- Mao, Ziliang; Liou, Shu-Hao; Khadka, Nimesh
- Biochemistry, Vol. 57, Issue 6
The surface science of nanocrystals
journal, January 2016
- Boles, Michael A.; Ling, Daishun; Hyeon, Taeghwan
- Nature Materials, Vol. 15, Issue 2
Substrate Interactions with the Nitrogenase Active Site
journal, March 2005
- Dos Santos, Patricia C.; Igarashi, Robert Y.; Lee, Hong-In
- Accounts of Chemical Research, Vol. 38, Issue 3
Activation Thermodynamics and H/D Kinetic Isotope Effect of the H ox to H red H + Transition in [FeFe] Hydrogenase
journal, September 2017
- Ratzloff, Michael W.; Wilker, Molly B.; Mulder, David W.
- Journal of the American Chemical Society, Vol. 139, Issue 37
Electron Transfer in Nitrogenase
journal, January 2020
- Rutledge, Hannah L.; Tezcan, F. Akif
- Chemical Reviews, Vol. 120, Issue 12
Crystallographic structure and functional implications of the nitrogenase molybdenum–iron protein from Azotobacter vinelandii
journal, December 1992
- Kirn, Jongsun; Rees, D. C.
- Nature, Vol. 360, Issue 6404
Establishing a Thermodynamic Landscape for the Active Site of Mo-Dependent Nitrogenase
journal, October 2019
- Hickey, David P.; Cai, Rong; Yang, Zhi-Yong
- Journal of the American Chemical Society, Vol. 141, Issue 43
Mechanism of Mo-Dependent Nitrogenase
journal, June 2009
- Seefeldt, Lance C.; Hoffman, Brian M.; Dean, Dennis R.
- Annual Review of Biochemistry, Vol. 78, Issue 1
Nitrogenase Bioelectrochemistry for Synthesis Applications
journal, November 2019
- Milton, Ross D.; Minteer, Shelley D.
- Accounts of Chemical Research, Vol. 52, Issue 12
Robust Photogeneration of H2 in Water Using Semiconductor Nanocrystals and a Nickel Catalyst
journal, November 2012
- Han, Z.; Qiu, F.; Eisenberg, R.
- Science, Vol. 338, Issue 6112
Controlled Assembly of Hydrogenase-CdTe Nanocrystal Hybrids for Solar Hydrogen Production
journal, July 2010
- Brown, Katherine A.; Dayal, Smita; Ai, Xin
- Journal of the American Chemical Society, Vol. 132, Issue 28
Role of Surface-Capping Ligands in Photoexcited Electron Transfer between CdS Nanorods and [FeFe] Hydrogenase and the Subsequent H 2 Generation
journal, December 2017
- Wilker, Molly B.; Utterback, James K.; Greene, Sophie
- The Journal of Physical Chemistry C, Vol. 122, Issue 1
Recent Progress in Photocatalysis Mediated by Colloidal II-VI Nanocrystals
journal, December 2012
- Wilker, Molly B.; Schnitzenbaumer, Kyle J.; Dukovic, Gordana
- Israel Journal of Chemistry, Vol. 52, Issue 11-12
Electron Transfer Kinetics in CdS Nanorod–[FeFe]-Hydrogenase Complexes and Implications for Photochemical H 2 Generation
journal, March 2014
- Wilker, Molly B.; Shinopoulos, Katherine E.; Brown, Katherine A.
- Journal of the American Chemical Society, Vol. 136, Issue 11
Synthesis and enzymatic photo-activity of an O 2 tolerant hydrogenase–CdSe@CdS quantum rod bioconjugate
journal, January 2014
- Hamon, C.; Ciaccafava, A.; Infossi, P.
- Chem. Commun., Vol. 50, Issue 39
Improvements to the APBS biomolecular solvation software suite: Improvements to the APBS Software Suite
journal, October 2017
- Jurrus, Elizabeth; Engel, Dave; Star, Keith
- Protein Science, Vol. 27, Issue 1
CONTIN: A general purpose constrained regularization program for inverting noisy linear algebraic and integral equations
journal, September 1982
- Provencher, Stephen W.
- Computer Physics Communications, Vol. 27, Issue 3
Relationships between Exciton Dissociation and Slow Recombination within ZnSe/CdS and CdSe/CdS Dot-in-Rod Heterostructures
journal, May 2017
- Grennell, Amanda N.; Utterback, James K.; Pearce, Orion M.
- Nano Letters, Vol. 17, Issue 6
Effect of Surface Ligands on Optical and Electronic Spectra of Semiconductor Nanoclusters
journal, June 2009
- Kilina, Svetlana; Ivanov, Sergei; Tretiak, Sergei
- Journal of the American Chemical Society, Vol. 131, Issue 22
Chemistry and Properties of Nanocrystals of Different Shapes
journal, April 2005
- Burda, Clemens; Chen, Xiaobo; Narayanan, Radha
- Chemical Reviews, Vol. 105, Issue 4
The Role of Ligands in Determining the Exciton Relaxation Dynamics in Semiconductor Quantum Dots
journal, April 2014
- Peterson, Mark D.; Cass, Laura C.; Harris, Rachel D.
- Annual Review of Physical Chemistry, Vol. 65, Issue 1
Multigrid solution of the Poisson?Boltzmann equation
journal, January 1993
- Holst, Michael; Saied, Faisal
- Journal of Computational Chemistry, Vol. 14, Issue 1
Substrate Interaction at an Iron-Sulfur Face of the FeMo-cofactor during Nitrogenase Catalysis
journal, October 2004
- Barney, Brett M.; Igarashi, Robert Y.; Dos Santos, Patricia C.
- Journal of Biological Chemistry, Vol. 279, Issue 51
Avogadro: an advanced semantic chemical editor, visualization, and analysis platform
journal, August 2012
- Hanwell, Marcus D.; Curtis, Donald E.; Lonie, David C.
- Journal of Cheminformatics, Vol. 4, Issue 1
Charge Transfer Dynamics between Photoexcited CdS Nanorods and Mononuclear Ru Water-Oxidation Catalysts
journal, February 2013
- Tseng, Huan-Wei; Wilker, Molly B.; Damrauer, Niels H.
- Journal of the American Chemical Society, Vol. 135, Issue 9
Mechanism of Molybdenum Nitrogenase
journal, January 1996
- Burgess, Barbara K.; Lowe, David J.
- Chemical Reviews, Vol. 96, Issue 7
The coordination chemistry of nanocrystal surfaces
journal, February 2015
- Owen, Jonathan
- Science, Vol. 347, Issue 6222
Numerical solution of the nonlinear Poisson-Boltzmann equation: Developing more robust and efficient methods
journal, March 1995
- Holst, Michael J.; Saied, Faisal
- Journal of Computational Chemistry, Vol. 16, Issue 3
Electron Transfer from the Nitrogenase Iron Protein to the [8Fe-(7/8)S] Clusters of the Molybdenum−Iron Protein
journal, January 1996
- Lanzilotta, William N.; Seefeldt, Lance C.
- Biochemistry, Vol. 35, Issue 51
Light-driven dinitrogen reduction catalyzed by a CdS:nitrogenase MoFe protein biohybrid
journal, April 2016
- Brown, K. A.; Harris, D. F.; Wilker, M. B.
- Science, Vol. 352, Issue 6284
Dissecting Electronic-Structural Transitions in the Nitrogenase MoFe Protein P-Cluster during Reduction
journal, March 2022
- Chica, Bryant; Ruzicka, Jesse; Pellows, Lauren M.
- Journal of the American Chemical Society, Vol. 144, Issue 13
Nitrogenase Complexes: Multiple Docking Sites for a Nucleotide Switch Protein
journal, August 2005
- Tezcan, F. A.
- Science, Vol. 309, Issue 5739
Exciton Localization and Dissociation Dynamics in CdS and CdS–Pt Quantum Confined Nanorods: Effect of Nonuniform Rod Diameters
journal, July 2014
- Wu, Kaifeng; Rodríguez-Córdoba, William; Lian, Tianquan
- The Journal of Physical Chemistry B, Vol. 118, Issue 49
Reduction of Substrates by Nitrogenases
journal, March 2020
- Seefeldt, Lance C.; Yang, Zhi-Yong; Lukoyanov, Dmitriy A.
- Chemical Reviews, Vol. 120, Issue 12